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Those of us who enjoy eating seafood are dismayed by the dreaded red tide, which renders some of our favorite prey toxic to us. A red tide occurs when dinoflagellates and other algae increase sharply in abundance, often in response to upwelling of nutrients from the ocean floor. Many of these dinoflagellates are red or brownish-red in color, so large numbers of them floating on or near the surface give the ocean its characteristic red color. These dinoflagellates produce toxic compounds (in particular neurotoxins) that pass through the food web, ultimately contaminating fish, molluscs and many other groups of species.

Red tide at Isahaya Bay, Japan. Credit: Marufish/Flickr.

Did toxicity arise in dinoflagellates to protect them from being eaten by predators – in particular by voracious copepods? The problem with this hypothesis is that copepods eat an entire dinoflagellate. Let’s imagine a dinoflagellate with a mutation that produces a toxic substance. At some point the dinoflagellate gets eaten, and the poor copepod consumer is exposed to the toxin. Maybe it dies and maybe it lives, but the important result is that the dinoflagellate dies, and its mutant genes are gone forever, along with the toxic trait. The only way toxicity will benefit the dinoflagellate individual, and thus spread throughout the dinoflagellate population, is if it increases the survival/reproductive success of individuals with the toxic trait. This can occur if copepods have some mechanism for detecting toxic dinoflagellates, and are therefore less likely to eat them.

Jiayi Xu and Thomas Kiørboe went looking for such a mechanism using 13 different species or strains of dinoflagellates that were presented to the copepod Temora longicornis. This copepod beats its legs to create an ocean current that moves water, and presumably dinoflagellates, in its direction, which it then eats. For their experiment, the researchers glued a hair to the dorsal surface of an individual copepod (very carefully), and they then attached the other side of the hair to a capillary tube, which was controlled by a micromanipulator. They placed these copepods into small aquaria, where the copepods continued to beat their legs, eat and engage in other bodily functions.

Twelve of the dinoflegellate strains were known to be toxic, though they had several different types of poison. Protoceratium reticulatum was a nontoxic control species of dinoflagellate. As you can see below, on average, copepods ate more of the nontoxic P. reticulatum than they did of any of the toxic species.

Average dinoflagellate biomass ingested by the tethered copepods. P. reticulatum is the nontoxic control. Error bars are 1 SE.

Xu and Kiørboe identified two major mechanisms that underlie selectivity by the copepod predator. In many cases, the copepod successfully captured the prey, but then rejected it (top graph below). For one strain of A. tamarense prey, and a lesser extent for K. brevis prey, the predator simply fed less as a consequence of reducing the proportion of time that it beat its feeding legs (bottom graph below).

Copepod feeding behavior on 13 dinoflagellate prey species. Top graph is fraction of dinoflagellates rejected, while bottom graph is the proportion of time the copepods beats its feeding legs in the presence of a particular species/strain of dinoflagellate.

If you look at the very first graph in this post, which shows the average dinoflagellate biomass consumed, you will note that both strains of K. brevis (K8 and K9) are eaten very sparingly. The graphs just above show that the copepod rejects some K. brevis that it captures, and beats its legs a bit less often when presented with K. brevis. However, the rejection increase and leg beating decreases are not sufficient to account for the tremendous reduction in consumption. So something else must be going on. The researchers suspect that the copepod can identify K. breviscells from a distance, presumably through olfaction, and decide not to capture them. This mechanism warrants further exploration.

One surprising finding of this study is that the copepod responds differently to one strain of the same species (A. tamarense) than it does to the other strains. Xu and Kiorbe point out that previous studies of copepod/dinoflagellate interactions have identified other surprises. For example, there are cases where a dinoflagellate strain is toxic to one strain of copepod, but harmless to another copepod strain of the same species. Also, within a dinoflagellate species, one strain may have a very different distribution of toxins than does a second strain. So why does this degree of variation exist in this system?

The researchers argue that there may be an evolutionary arms race between copepods and dinoflagellates. The copepod adapts to the toxin of co-occurring dinoflagellates, becoming resistant to the toxin. This selects for dinoflagellates that produce a novel toxin that the copepod is sensitive to. Over time, the copepod evolves resistance to the second toxin as well, and so on… Because masses of ocean water and populations of both groups are constantly mixing, different species and strains are exposed to novel environments with high frequency. Evolution happens.

If you’re ever feeling sorry for yourself, you should know that things could have been much worse; you could have been the brown seaweed, Silvetia compressa. So many problems! Ocean waves come crashing over you, threatening to pull you off your life-sustaining substrate. Ocean tides recede, exposing you to harsh sun and dangerously dry conditions. Perhaps worst of all, the fearsome predator Tegula funebralis eats away at your body, and you are powerless to defend yourself from its savage ravages.

As it turns out, Silvetia is not so powerless after all. After being partially grazed by Tegula, the seaweed can induce defenses that reduce its palatability. From prior work, Emily Jones noticed that seaweed from northern California shorelines was much more sensitive to grazing than was seaweed from southern California shorelines. It took fewer grazing snails to elicit palatability reduction in northern Silvetia than it did in southern Silvetia. She decided to focus her PhD work with Jeremy Long on documenting these geographic differences, and figuring out why they exist.

Environmental conditions vary along the California coast. Northern seaweed populations experience cooler temperatures (air ~5-20 °C; water ~10-12 °C) and more nutrients (nitrate levels up to 40 umol/L) than do southern populations (air 5-37 °C; water ~14-20 °C; nitrate levels < 2 umol/L). In addition, Jones and Long surveyed Tegula abundance at three northern California and three southern California sites, counting every snail in 20 quadrats placed in the low, mid and high intertidal zone at each of the six sites (360 0.25 X 0.25m quadrats in total) . They discovered that seaweed was much more likely to encounter Tegula along northern coastlines.

Given these differences in snail abundance, we can now understand why Silvetia is more sensitive in its northern range to Tegula grazing. But how strong are these differences in sensitivity? Jones and Long developed a simple paired-choice feeding preference assay to test for differences in palatability. At each location (north and south), the researchers gave test snails a choice between feeding on seaweed that had been previously grazed by either 1, 4, 7, 10 or 13 Tegula snails, or to feed on seaweed with no grazing history. The test snails grazed for five days, and the researchers measured the amount of seaweed consumed for each group. They discovered that even a little bit of previous grazing (the 1-snail treatment) made northern test snails prefer non-grazed northern Silvetia, while only high levels of previous grazing (the 10 and 13-snail treatments) had similar effects on southern snails tested on southern Silvetia.

These findings raised the question of whether the cooler and more nutrient-rich environmental conditions at the northern site were somehow causing this difference in consumption of previously-grazed seaweed. The researchers designed a series of common garden experiments at the Bodega Marine Laboratory, in which seaweed from both locations were tested in the same environment. Silvetia was exposed to grazing by two snails, or by no snails for 14 days. When test snails were given the choice of non-grazed or previously-grazed northern Silvetia, they much preferred eating non-grazed Silvetia. In contrast, they showed no preference when given a similar choice between non-grazed or previously-grazed southern Silvetia. This indicates that seaweed from the north are responding more to grazing by reducing palatability than are seaweed from the southern locations.

Amount of previously-grazed and non-grazed northern and southern Silvetia eaten by Tegula in paired choice tests.

In theory, there could be a tradeoff between induced defenses, such as reduction in palatability in response to grazing, and constitutive defenses, which an organism expresses all of the time. Examples of constitutive defenses are thorns or spines in plants, and cryptic coloration or body shape in many insects. Jones and Long found no evidence for such a tradeoff; in contrast southern Silvetia actually had lower levels of constitutive defenses, as both northern and southern Tegula strongly preferred eating southern Silvetia in paired choice tests.

Amount of northern and southern Silvetia eaten by northern and southern Tegula in paired choice tests.

These geographic differences in seaweed sensitivity to grazing are probably due to long-term differences in environmental history. Southern Silvetia seaweeds live in stressful conditions (high temperatures and low nutrients), and the physiological cost of mounting an induced defense against low and moderate levels of grazing may be too high to be worthwhile. We also don’t know what the overall grazing rates are in the north versus the south, and importantly, how variable the grazing rates are in each location. Highly variable grazing rates would select for a strong set of induced responses, which could be turned on and off as needed, allowing seaweed, or any plant, to defend itself against new or more hungry herbivores moving into their environment.

Many plants shed their young embryos (seeds) into the soil where they may accumulate in a dormant (non-growth) state over years before germinating (resuming growth and development). Ecologists describe this collection of seeds as a seed bank. Marina LaForgia describes how scientists were able to germinate and grow to maturity some 32,000 year old Silene stenophylla seeds that was stashed, probably by an ancient squirrel, in the permafrost! With increased climatic variation predicted by most climate models, she wanted to know how environmental variability might affect germination of particular groups of species within a community. In addition, she and her colleagues recognized that most ecological studies investigate community responses to disturbances by looking at the aboveground species. It stands to reason that we should consider the below-surface seed bank as a window to how a community might respond in the future.

Some seedlings coming up from the seed bank. Credit:Marina LaForgia.

Seed banks can be viewed as a bet-hedging strategy that spreads out germination over several (or many) years to reduce the probability of catastrophic population decline in response to one severe disturbance, such as drought, flood or fire. In some California annual grassland communities, species diversity is dominated by annual forbs – nonwoody flowering plants that are not grasses. Many forbs produce seeds that can lie dormant in the seed banks for several years. Though these forbs are the most diverse group, there are also about 15 species of exotic annual grasses that dominate the landscape in abundance and cover. These grasses dominate because they produce up to 60,000 seeds per m2, they grow very quickly, and they build up a layer of thatch that suppresses native forbs. However, seeds from these grasses cannot lie dormant in the seed bank for very long.

Area of field site dominated by Delphinium (purple flower) and Lasthenia (yellow flower). Looking closely you can also see some tall grasses rising. Credit Marina LaForgia.

How is drought affecting these two major components of the plant community? LaForgia and her colleagues answered this question by collecting seeds from a northern California grassland at the University of California McLaughlin Natural Reserve in fall 2012 (beginning of the drought) and fall 2014 (near the end of the drought). They used a 5-cm diameter 10-cm deep cylindrical sampler to collect soil and associated seeds from 80 different plots. The researchers also used these same plots to estimate aboveground-cover, and to identify the aboveground species that were present. The research team germinated and identified more than 11,000 seeds.

Plants germinating in the greenhouse. Credit Marina LaForgia.

The researchers knew from previous work on aboveground vegetation that exotic annual grasses declined very sharply in response to drought. In contrast, the native forbs did relatively well, in part depending on their specific leaf area (SLA) – a measure of relative leaf size, with low SLA plants conserving water more efficiently. It seemed reasonable that these same patterns would be reflected belowground. Recall that most grass seeds are incapable of extended dormancy, while many forbs can remain dormant for several years. Consequently, LaForgia and her colleagues expected that grass abundance in the seed bank would decline more sharply than would forb abundance. In addition, they expected that high SLA forbs would not do as well as low SLA forbs during drought.

The researchers discovered very sharp differences between the two groups over the course of the drought. Exotic annual grasses declined sharply in the seed bank, while native annual forb abundance tripled. Aboveground cover of grasses declined considerably, while aboveground cover of forbs increased modestly. Clearly the exotic grasses were suffering from the drought, while the forbs were doing quite well.

(a) Seed bank abundance of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). (b) Percent cover of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). Data are based on samples from 80 plots. Error bars indicate one standard error.

We can see these differences on an individual species basis, with most of the grasses declining modestly or sharply in abundance, while most of the forbs increased.

Mean change in seed bank abundance per species based on 15 exotic grass species and 81 native forb species.

It is not surprising that the grasses do so poorly during the drought. Presumably, less water causes poorer germination, growth, survival and seed production. In addition, because grass seeds have a low capacity for dormancy, grass abundance will tend to decrease in the seed bank very quickly with such a low infusion of new seeds.

But why are the forbs actually doing better with less water available to them? One explanation is that grass abundance and cover declined sharply, causing the forbs to experience reduced competition with grasses that might otherwise inhibit their growth, development and reproductive success. The tripling of native forbs in the seed bank was much greater than the 14% increase in aboveground forb cover. The researchers reason that the drought caused many of the forb seeds to remain dormant, leading to them building up in the seed bank. This was particularly the case for low SLA forbs, which increased much more than did high SLA forbs in the seed bank.

We can understand exotic grass behavior in the context of their place of origin – the Mediterranean basin, which tends to have wet winters. In that environment, natural selection favored individuals that germinated quickly, grew fast and made lots of babies. Since their introduction to California in the mid 1800s, 2014 was the driest year on record. It will be fascinating to see if these exotic grasses can recover when, and if, wetter conditions return. Can we bank on it?

There was a time in the mid-Pleisticine when a photo of an ecological event was an awesome novelty, and a movie of an ecological event even more so. Dodderers of an ecological bent (myself included), can vividly recall viewing a series of photos or a movie, either in a seminar or in an ancient ecology text, of a blue jay consuming a monarch butterfly, Danaus plexippus. Consumption is immediately followed by explosive vomiting, as the cardenolides within the monarch butterfly claim another victim. The monarch sequesters these cardenolide toxins from its larval food (milkweed), and incorporates them into its tissues as a means of protecting itself from predators – presumably blue jays learn from this very aversive experience. I should point out that the individual sacrificial butterfly enjoys no fitness from this learning event – which raises some evolutionary questions we will not explore at the present.

Five instars (stages of development) of monarch caterpillars on a milkweed leaf. Credit: Karen Oberhauser

Rather we turn our attention to the relationship between milkweed, monarchs, and climate change. In several places in this blog we’ve talked about how climate change has influenced the behavior or physiology of a single species. For example, my first blog (Jan 31, 2017) discusses how increasing temperatures create more females in a loggerhead turtle population. But there are fewer studies that explore how climate change influences the ecological landscape, ultimately affecting interactions between species. Along these lines, Matt Faldyn wondered if increased air temperature would change the chemical constitution of milkweed in a way that might influence monarch populations. As he describes, “With milkweed toxicity, there is a ‘goldilocks’ zone where monarchs prefer to feed on milkweed that produce enough toxins in order to sequester these (cardenolide) chemicals as an antipredator/antiparasite defense, while also avoiding reaching a tipping point of toxicity where feeding on very toxic milkweeds negatively impacts monarch fitness.” He expected that at higher temperatures, milkweed would become stressed, and be physiologically unable to sustain normal levels of cardenolide production.

Monarch butterfly feeds on a native milkweed, Asclepias incarnata. Credit: Teune at the English Language Wikipedia.

For their research, Faldyn and his colleagues worked with two milkweed species. Asclepias incarnata is a common, native milkweed found throughout the monarch butterfly’s range in the eastern and southeastern United States. Asclepias curassavica is an exotic species that has become established in the southern United States. In contrast to A. incarnata, A. curassavica does not die back over the winter months; consequently some monarch populations are no longer migratory, relying on A. curassavicato provide them with a year round food supply.

To protect against herbivory, milkweeds have two primary chemical deterrants: (1) the already-mentioned cardenolides, which are toxic steroids that disrupt cell membrane function, and (2) release of sticky latex, which can gum up caterpillar mouthparts and actually trap young caterpillars.

The researchers wanted to simulate climate change under field conditions, so they created open-top chambers with plexiglass plates that functioned much like mini-greenhouses, into which they placed one milkweed plant that was covered with butterfly netting. This setup raised ambient temperatures by about 3°C during the day and 0.2°C at nighttime. Control plots were single milkweed plants with butterfly netting. Half of the plants were native milkweed, and the other half were the exotic species.

For their experiments, Faldyn and his colleagues introduced 80 monarch caterpillars (one per plant) and allowed them to feed normally until they pupated. Pupae were brought into the lab and allowed to metamorphose into adults.

At normal (ambient) temperatures, monarchs survived somewhat better on exotic milkweed. But at warmer temperatures, there is a strikingly different picture. Monarch survival is unaffected by warmer temperatures on native milkweed, but is sharply reduced by warmer temperatures on exotic milkweed (top graph below). The few that managed to survive warm temperatures on exotic milkweed grew much smaller, based on their body mass and forewing length (middle and bottom graph below)

Both milkweed species increased production of both types of chemicals over the course of the experiment. But by the end of the experiment, the exotic species released 3-times the quantity of latex and 13-times the quantity of cardenolides than did the native milkweed species.

Average amount of latex released at the beginning and end of the experiment. Error bars are 95% confidence intervals.

Average cardenolide concentration at the beginning and end of the experiment.

The researchers argue that the exotic milkweed, Asclepias curassavica, may become an ecological trap for monarch butterflies, in that it attracts monarchs to feed on it, but will, under future warmer conditions, result in dramatically reduced monarch survival. Interestingly, these results are not what Faldyn originally expected; recall that he anticipated that temperature-stressed plants would reduce cardenolide production. The tremendous increase in cardenolide production in exotic milkweed at warmer temperatures may simply be too much toxin for the monarchs to process. The researchers predict that as climate warms, milkweed ranges will expand further north into Canada, and lead to northward shifts of monarch populations as well. They urge nurseries to emphasize the distribution of native rather than exotic milkweed, so that monarchs will be less likely to become victims of this ecological trap.

As she was preparing to do her dissertation research on the interactions between the Asian chestnut gall wasp, the chestnut blight disease and the European chestnut, Pilar Fernandez-Conradi read a lot of papers about fungal-insect-plant interactions. She was impressed by the diversity of outcomes that resulted when plants were attacked by both insects and fungi, and wondered whether there were any generalities to glean from these research findings. She asked two basic questions. First, if a plant is infected by a fungus, is it more or less likely to be attacked by insects than is an uninfected plant? Second, does an insect that attacks a fungal-infected plant perform better or worse than it would have on an uninfected plant?

Three-way interaction between the chestnut tree, the chestnut gall wasp, and the fungus Gnomopsis castanea. Female wasps induce the plant to create galls, which house developing larvae. Green globular galls (with a hint of rose-color) have not been infected by a fungus, while the very dark tissue is the the remains of a gall that was attacked by the fungus. Credit: Pilar Fernandez-Conradi.

Fernandez-Conradi and her colleagues thought they were more likely to discover a negative effect of fungal infection on the preference and performance of herbivorous insects. Several studies had shown that nutrient quantity and quality of host plants is reduced by fungal infection, so it makes sense that insects would avoid infected plants. But the researchers also knew that fungal infection can, in some cases, actually increase the sugar concentration of some plants, so insects might prefer those plants and also develop more rapidly on them. In addition, fungal infection can induce chemical defenses in plants that might make them less palatable to insects, or alternatively, fungal infection could weaken plant defenses making them more palatable to attacking insects.

To resolve this conundrum, Fernandez-Conradi and her colleagues did a meta-analysis, of the existing literature, identifying 1113 case studies based on 101 papers. To be considered in the meta-analysis, all of the studies had to meet the following criteria: (1) report insect preference or performance on fungal-infected vs. uninfected plants, (2) report the Genus or species of the plant, fungus and insect, (3) report the mean response and a measure of variation (standard error, standard deviation or variance). The measure of variation allows researchers to calculate the effect size, which calculates the strength of the relationship that is being explored. The researchers found that, in general, insects avoid and perform worse on infected plants than they do on uninfected plants.

Mean effect size of insect preference and performance (combined) in response to fungal infection infection. Error bars are 95% confidence intervals (CIs). In this graph, and the next two graphs as well, a solid data point indicates a statistically significant effect. You can also visually test for statistical significance by noting that the error bar does not cross the dashed vertical line that represents no effect (at the 0.0 value). The negative value indicates that insects respond negatively to fungal infection.

Fernandez-Conradi and her colleagues then broke down the data to explore several questions in more detail. For example, they wondered if the type of fungus mattered. For their meta-analysis, they considered three types of fungi with different lifestyles: (1) biotrophic pathogens that develop on and extract nutrients from living plant tissues, (2) necrotrophic pathogens that secrete enzymes that kill plant cells, so they can develop and feed on the dead tissue, and (3) endophytes that live inside living plant tissue without causing visible disease symptoms.

Effect of fungus lifestyle on insect performance. k = the number of studies. Different letters to the right of CIs indicate significant differences among the variables (lifestyles).

The meta-analysis showed an important fungus-lifestyle effect (see the graph to your left). Insect performance was strongly reduced in biotrophic pathogens and endophytes, but not in necrotrophic pathogens, where insect performance actually improved slightly (but not significantly). The researchers point out that biotrophic pathogens and endophytes both develop in living plant tissues, while necrotrophic pathogens release cell-wall degrading enzymes which can cause the plant to release sugars and other nutrients. These nutrients obviously benefit the fungus, but can additionally benefit insects that feed on the plants.

To further explore this lifestyle effect, Fernandez-Conradi and her colleagues broke down insect response into performance and preference, focusing on chewing insects, for which there were the most data. Insects showed lower performance on and reduced preference (i.e. increased avoidance) for plants infected with biotrophic pathogens. They also performed equally poorly on endophyte-infected plants, but did not avoid endophyte-infected plants (see graph below). This was surprising since you would expect natural selection to favor insects that can choose the best plants to feed on. The problem for insects may be that endophytic infection is basically symptomless, so the insects may, in many cases, be unable to tell that the plant is infected, and likely to be less nutritionally rewarding.

Effects of fungal infection on preference and performance of chewing insects. k = the number of studies. Different letters to the right of CIs indicate significant differences among the variables. Variables that share one letter have similar effect sizes.

Many ecological studies deal with two interacting species: a predator and a prey, or a parasite and its host. Fernandez-Conradi and her colleagues remind us that though two-species interactions are much easier to study, many important real-world interactions involve three or more species. Their meta-analysis highlights that plant infection by pathogenic and endophytic fungi reduces the performance and preference of insects that feed on these plants. But fungus lifestyle plays an important role, and may have different effects on performance and preference. Their meta-analysis also suggests other related avenues for research. For example, how are plant-fungus-insect interactions modified by other species, such as viruses, bacteria and parasitoids (an animal that lives on or inside an insect, and feeds on its tissues)? Or, what are the underlying molecular (hormonal) mechanisms that determine the response of the plant to fungal infection, and to insect attack? Finally, how does time influence both plant and insect response? If a plant is recently infected by a fungus, does it have a different effect on insect performance and preference than does a plant that has suffered from chronic infection. There are very few data on these (and other) questions, but they are more likely to get pursued now that some basic relationships have been uncovered.

While it would be awesome if parrotfish were named for their conversational abilities, it turns out that they earn their moniker for their specialized teeth that are fused together for scraping algae from coral, thus resembling a parrot’s beak. Despite lacking verbal skills these fish are incredible. Approximately 100 species occupy reefs, rocky coastlines and eelgrass meadows in tropical and subtropical waters. Many species are sequential hermaphrodites, beginning life as females and then changing into males after reaching a certain size. While female reproductive success is limited by the number of eggs she can produce, male reproductive success can be much higher if he can fertilize the eggs of many females. So if a parrotfish transitions into a large male, and can control access to numerous females, he will enjoy greater reproductive success than if he had remained a female.

Two Chlorurus spilurus parrotfish show off their teeth and colors. The large colorful fish on the right is a male, while the smaller darker fish to his left is a female. Credit: Brett Taylor.

Phenotypic plasticity describes the ability of an individual with a particular genetic makeup to vary in a variety of traits (such as what it looks like, or how it behaves) in response to different environmental conditions. About 15 years ago, Nick Gust’s PhD research on tropical reef fish revealed that tremendous variation in parrotfish traits existed over a distance of a few kilometers. But what causes this variation? When funding became available, Brett Taylor jumped at the opportunity to pinpoint the causes, focusing on the diverse parrotfish community in the Great Barrier Reef (GBR).

Eastern slope of the Great Barrier Reef hosts a diversity of fish and coral species. Credit: Brett Taylor.

Taylor and his colleagues surveyed 82 sites within 31 reefs across 6 degrees of latitude in the northern GBR. To standardize data collection, divers, armed with a multitude of cameras and GPS devices, swam at a standardized rate (about 20 meters/minute) for 40 minutes per survey, recording each parrotfish along a 5 m wide swath. They collected data about the habitat and the environment, about the physical traits of each individual parrotfish (such as size and sex), and about the type and abundance of parrotfish and their predators present at each site.

Researcher takes notes while conducting a dive. Credit Kendra Taylor.

The researchers wanted to identify what factors influenced growth rate, maximum body size, and the size at sex change, and how these factors related to the parrotfish mating system. Four species of parrotfish were sufficiently abundant across the GBR to allow researchers to do this type of analysis.

Four parrotfish species abundant along exposed outer shelf (yellow sites) and protected inner shelf (blue) regions of the Great Barrier Reef. Males are larger and more colorful.

The GBR varies structurally across a relatively small spatial scale of 40 – 100 km, with outer shelf regions (eastern) exposed to wave action, and inner shelf regions (western) relatively protected. All four species tended to change sex at a larger size in protected sites than they did at exposed sites. However, the differences are only compelling for two of the species: C. spilurus and S. frenatus. There were fewer data points for the other two species, so it is possible (but unknown) that they too would show a more pronounced trend if more data were available.

Proportion terminal phase (sex-changed males) in relation to body size (measured to the fork of the tail) in exposed (yellow) and sheltered (blue) sites.

Not surprisingly, parrotfish grew larger in protected areas. Presumably, less wave action provided a more benign environment for rapid growth, both of parrotfish and their preferred food items (algae growing on rocks and coral).

The researchers were somewhat surprised that most other factors, such as latitude, coral cover, sea surface temperature, and predator abundance, had very little effect on the size at sex change. Rather, the size at sex change appears to be strongly influenced by the local size distribution. In protected habitats, parrotfish grow large and change sex at a large size, while in exposed habitats, parrotfish are smaller, and change sex at a smaller size.

But sex is never simple. Nick Gust’s PhD research showed that C. spilurus had different patterns of sexual allocation in protected vs. exposed areas. In protected areas, the mating system is haremic, with a large male defending a territory and servicing a harem of females. In exposed areas, the mating system is mixed; there still are large territorial males with their harems, but they compete with many more small males, and group spawning is much more prevalent. Theoretically, the presence of these small males may make it less worthwhile for a female to transition into a male, and may influence the optimal size for transitioning in exposed reefs. Given that we still don’t know the mating system details of the other parrotfish in this study, it will be fascinating to see if they too show similar patterns of haremic vs. mixed mating systems in relation to habitat structure.

We tend to think of plants as victims – after all any interested herbivore can simply walk, fly or crawl over to its favorite plant, and begin munching. But not so fast! In reality, plants have a variety of ways they can make life difficult for potential herbivores. Plants can escape herbivores by simply growing in places that are not easily accessible (such as in cracks, or high enough to be out of a herbivore’s reach) or by growing at a time of year when herbivores are away from the plant’s habitat. Plants also use mechanical defenses such as thorns or a diverse array of chemical defenses to thwart overzealous herbivores. A third approach – tolerance – can take many forms. For example, following attack by a herbivore some plants can increase photosynthetic rates or reduce the time until seed production . Tommy Lennartsson and his colleagues were interested in a particular form of tolerance that ecologists call overcompensation, in which damaged plants produce more seeds than undamaged plants.

Overcompensation is an evolutionary puzzle, because undisturbed plants produce fewer offspring than partially eaten plants. That outcome seems to fly in the face of the scientific principle that natural selection favors individuals with traits that promote reproductive success. Lennartsson and his colleagues investigated this evolutionary puzzle by comparing two subspecies of the herbaceous field gentian Gentianella campestris. The first subspecies, Gentianella campestris campestris (which we’ll just call campestris), has relatively unbranched shoot architecture when intact, growing to about 20 cm tall, but produces multiple fruiting branches when the dominant apical meristem is eaten. The second subspecies, Gentianella campestris islandica (which we’ll call islandica), is much shorter (about 5-10 cm tall), and always has a multi-branched architecture.

Two subspecies of field gentian – campestris (left) and islandica (right).

Environmental conditions and soils can vary dramatically, even on a small spatial scale. The field site was a gently-sloped grassland in Sweden that had coarser, dryer soil on the ridge, and finer, wetter and richer soil in the valley. This created a productivity gradient, with taller vegetation in the valley. The average height of all the vegetation was 15 cm in the high-productivity valley, 10 cm on the medium-productivity slope and 5 cm on the low-productivity ridge.

The researchers used this natural variation to set up an experiment that would allow them to explore hypotheses about why an undisturbed campestris is less successful than one that is partially-eaten. One hypothesis (the overcompensation hypothesis) is that campestris restrains branching to conserve resources, so that when it is grazed it has plenty of resources in reserve to be used for regrowth and the production of prolific branches, flowers and seeds. Limited branching and limited seed production of ungrazed campestris are simply a cost of tolerance, while overcompensation after damage maximizes reproductive success. A second hypothesis (the competition hypothesis) is that restrained branching allows the plant to grow tall, so it can compete better in ungrazed pastures than can the much shorter islandica. These two hypotheses are not mutually exclusive.

To test these two hypotheses, the researchers set up 2 X 2 meter experimental plots in the valley (18 plots), slope (12 plots) and the ridge (6 plots). They planted 2000 seeds per subspecies in each plot, which ultimately yielded about 20 plants of each subspecies per plot. Of course there were many other neighboring plant species in these plots. In the high productivity plots (valley), the neighboring plants in six plots were clipped to a height of 12 cm, six plots to 8 cm and six plots to 4 cm. In the medium productivity plots (which naturally only grew to 10 cm), the researchers cut neighboring plants to 8 cm in 6 plots and 4 cm in six plots. Finally, in the low productivity plots, the researchers cut neighboring plants to 4 cm in all six plots. In mid July, half of the gentian plants in each plot were clipped to the same height as the surrounding vegetation, while the remainder were not clipped.

Experimental plots from the valley (left), slope (middle) and ridge (right). Black squares represent plots where neighboring plants were clipped to 12 cm, grey squares to 8 cm, and clear squares to 4 cm. Squares with slashes through them (left) represent plots that were used for a different purpose.

The beauty of this experimental design, is that by counting seeds, the researchers could assess the reproductive success of both subspecies under conditions of high competition (when surrounded by tall neighbors) and low competition (when surrounded by shorter neighbors). At the same time, clipping the two subspecies allowed the researchers to simulate grazing in these different competitive environments. Lennartsson and his colleagues found that unclipped islandica did better than unclipped campestris when surrounded by short or medium height neighbors, but that islandica success plummeted when the neighbors were very tall (see the left graph below). Campestris reproductive success also dropped when surrounded by tall competitors, but not as much as did islandica, so that campestris produced twice as many seeds than islandica in the high competition environment (also the left graph).

When plants were clipped to simulate grazing, campestris outperformed islandica in all three competitive environments. Campestris actually produced more seeds when it was clipped than when it was not clipped in the low and medium competition environments. Thus campestris overcompensated for grazing under conditions of low and moderate competition (see the right graph below).

The researchers collected data on growth rates, development, survival probabilities and reproductive success for both species under conditions of being clipped or unclipped at different levels of competition. They then used these data to create a population growth model in relation to the percentage of grazing (damage risk) at different levels of productivity. In these graphs, a stochastic growth rate of 1.0 (on the y-axis) indicates that the population is stable, above 1.0 indicates it will increase and below 1.0 indicates a declining population.

Population growth rate of both subspecies in relation to damage risk at different levels of productivity. These models predict that the population will increase at growth rates above the dotted line (growth rate = 1.0) and decline below the dotted line.

This model shows that in high productivity environments, campestris always does better than islandica (top graph). However, the model predicts that islandica will decline at any damage level (note in the top graph that all islandica damage values yield a growth rate below 1.0), while campestris will also decline except for very high damage risks. In medium and low productivity populations (middle and bottom graphs), islandica does better than campestris when damage risk is low, but the reverse is true at high damage risk.

So how do these results relate to the two hypotheses for why an undisturbed campestris is less successful than one that is partially-eaten. Campestris overcompensated for damage by producing more seeds and having positive population growth under most levels of productivity. In contrast, islandica undercompensated when damaged, but produced more seeds than campestris when ungrazed, except for in the high productivity environment. These differences in responses support the hypothesis that restrained branching is favored by natural selection in environments where damage from grazing is common (the overcompensation hypothesis). But, the superior performance by campestris in productive ungrazed environments supports the competition hypothesis.

Can we generalize these findings to other plants? Lennartsson and his colleagues point out that many short-lived grassland plants can’t grow tall enough to be effective competitors for light. These plants are thus restricted to environments where the surrounding plants are not very tall. Two factors commonly create conditions where there are short neighboring plants: grazing and unproductive (low nutrient) soils. When grazing is widespread, tolerance mechanisms such as overcompensation are favored by natural selection. When soils are unproductive, unrestrained branching is favored. Therefore, Gentianella campestris provides us with a natural experiment for testing hypotheses about how natural selection acts on plants to promote their reproductive success in a variable environment.